Bogus Visual Feedback Alters Onset of Movement-Evoked Pain in People With Neck Pain

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Bogus visual feedback alters movement-evoked pain onset

in people with neck pain

Journal: Psychological Science

Manuscript ID: PSCI-14-1100.R1

Manuscript Type: Research article

Date Submitted by the Author: 30-Sep-2014

Complete List of Authors: Harvie, Daniel; The University of South Australia, The Sansom Institute for Health Research Broecker, Markus; The University of South Australia, The Wearable Computer Lab Smith, Ross; The University of South Australia, The Wearable Computer Lab

Meulders, Ann; University of Leuven, Research Group on Health Psychology, Department of Psychology Madden, Victoria; The University of South Australia, The Sansom Institute for Health Research Moseley, G; The University of South Australia, The Sansom Institute for Health Research; Neuroscience Research Australia, ; PainAdelaide,

Keywords: Perception, Virtual Reality, Threat, Motion Perception

Manuscript under review for Psychological Science

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Running head: VISUAL FEEDBACK ALTERS MOVEMENT-EVOKED PAIN

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Bogus visual feedback alters movement-evoked pain onset in people with neck pain

Daniel S. Harvie, Markus Broecker, Ross T. Smith, Ann Meulders, Victoria J. Madden, G.

Lorimer Moseley

University of South Australia, Australia

Author Note

Daniel S. Harvie, Victoria J. Madden of the Samson Institute for Health Research, University

of South Australia, and PainAdelaide, Adelaide, Australia; Markus Broeker, Ross Smith of

The Wearable Computer Lab, University of South Australia, Australia; Ann Meulders of the

Research Group on Health Psychology, Department of Psychology, University of Leuven,

Belgium and Center for Excellence on Generalization Research in Health and

Psychopathology, University of Leuven, Belgium; G. Lorimer Moseley of the Samson

Institute for Health Research, University of South Australia, PainAdelaide, and Neuroscience

Research Australia, Australia.

G. Lorimer Moseley is supported by an NHMRC Principal Research Fellowship ID

1061279. This study supported by NHMRC Grant ID 1047317. Ann Meulders is supported

by a postdoctoral research grant of the Research Foundation-Flanders, Belgium (FWO-

Vlaanderen) Grant ID 12E3714N and an EFIC-Grünenthal research grant E-G-G ID

169518451. The authors wish to thank Julie Peacock, Jonathon Schubert, William Kuang,

Ellie Magarey (Marion Physiotherapy), Di Wilson, Peter Roberts, Eva Boesch and Toby

Moen (Roberts Physiotherapy), Jason Collins and Glen Kocher (Northcare Physiotherapy) for

assistance with recruitment and Anthony Ikiosoglous for assistance with blinded data

extraction.

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Correspondence concerning this article can be addressed to Lorimer Moseley, University of South Australia, GPO Box 2471, Adelaide, South Australia 5001.

E-mail: [email protected]

Abstract

Pain is a protective perceptual response shaped by contextual, psychological and sensory

inputs that suggest danger to the body. Sensory cues suggesting that a body part is moving

towards a painful position, may credibly signal danger and thereby modulate pain. In this

experiment, we used virtual reality to investigate whether manipulating visual-proprioceptive

cues could alter movement-evoked pain, in 24 people with neck pain. We hypothesised that

pain would occur at a lesser degree of head rotation when visual feedback overstated true

rotation, and at a greater degree of rotation when visual feedback understated true rotation.

Our hypothesis was clearly supported: when vision overstated the amount of rotation, pain

occurred at 7% less rotation, and when vision understated rotation, pain occurred at 6% more

rotation. We conclude that visual-proprioceptive information modulates movement-evoked

pain threshold. This suggests that stimuli that become associated with pain, can themselves

trigger pain.

Keywords: pain, perception, virtual reality, redirected walking, illusions, body

representation, movement, multisensory processing.

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Bogus visual feedback alters movement-evoked pain onset in people with neck pain

Introduction

Over the past three decades, the multidimensional nature of pain and nociception has been

elucidated by research revealing that many factors, from sensory (Moseley & Arntz, 2007),

cognitive (Wiech, Ploner, & Tracey, 2008; Brooks & Tracey 2005), and emotional (Wiech &

Tracey, 2009; Brooks & Tracey 2005) domains, modulate pain. Critically, non-nociceptive

somatosensory information can both modulate and evoke pain (Acerra & Moseley, 2005;

Derbyshire, 2004; Arntz & Claassens, 2004), suggesting that pain is an ‘information-evoked’

response. The sensory cues capable of contributing to pain have not been well explored,

although some authors suggest that any information that leads the brain to conclude that the

body is in danger may evoke pain (Merksey & Bogduk, 1994; Moseley, 2003; Price, 1999;

Arntz & Claassens, 2004).

This suggestion is not surprising, given what is known about other perceptual

domains, where sensory elements combine into meaningful wholes. When perceiving a table,

for example, we are not aware of individual colours, edges and shapes, but rather the unified

whole (Goldstein, 2013; Hochstein & Ahissar, 2002; Weiten, 2007). There is ample

psychological research investigating the principles underlying this sensory integration,

particularly with respect to vision (Wagemans et al., 2012), but such principles have received

scant attention in the study of pain.

Pain serves a protective function, so it is natural to think that non-nociceptive sensory

information might help to determine whether pain is an appropriate perceptual response. For

example, nociceptive input from a small laceration may evoke pain only after visual


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information is added. Experimentally, non-nociceptive cues contingently paired with

nociceptive input (through classical conditioning) modulate the pain evoked by subsequent

nociceptive stimulation (Atlas, Bolger, Lindquist, & Wager, 2010; Keltner et al., 2006;

Koyama, McHaffie, Laurienti, & Coghill, 2005). It is assumed that, after such pairing, the

non-nociceptive cues become signals of body-related threat and thus join the suite of

information used by the brain to determine whether pain is an appropriate protective

perceptual response. This view is supported by experimental evidence showing that the pain

evoked by a nociceptive stimulus is affected by the meaning of both the nociceptive stimulus

and other non-nociceptive stimuli that are presented at the same time (Arntz & Claassens,

2004; Moseley & Arntz, 2007).

Very few studies have investigated the relationship between non-nociceptive

information and clinical pain. One study showed that people with complex regional pain

syndrome (CRPS) experienced pain when given visual input (via a mirror) suggesting touch,

despite the absence of actual touch (Acerra & Moseley, 2005). However, this procedure did

not evoke pain in a group with non-CRPS neuropathic hand pain (Krämer, Seddigh, Moseley,

& Birklein, 2008). One might therefore suggest that non-nociceptive cues are only important

in certain conditions. But if pain is ‘information-evoked’ — as we contend that it is — then a

threshold of relevant information, nociceptive and/or non-nociceptive, must be reached in

order to evoke pain. This idea is untested, but if relevant non-nociceptive input does affect

the amount of additional input required to evoke pain, it would effectively constitute a change

in pain threshold. One type of input that might have such influence is proprioceptive

information about specific movements and body positions. This is especially likely when a

vulnerable body part needs to be protected. In the instance of a neck injury, for example,

specific proprioceptive information might predict nociceptive stimulation and thus contribute

to defensive responses including pain.


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In the present study, we tested the hypothesis that proprioceptive information might

contribute to pain by examining how altering visual-proprioceptive feedback during neck

rotation affects the range of motion to the onset of pain (movement-evoked pain threshold) in

longstanding neck pain sufferers. Using the ‘information-based’ view of pain, we

hypothesised that pain would occur earlier when visual-proprioceptive information overstated

real-world rotation, and later when visual-proprioceptive information understated real-world

rotation.

Methods

Participants

Twenty four individuals (6 males; mean age ± SD = 45 ± 15 years) volunteered to

participate in this study. Sample size was determined a priori to enable detection of a small-

medium effect size (f = 0.2) with 80% power, conservatively assuming a 60% correlation

among repeated measures. The average duration of complaint was 11 years (SD = 11; range:

2 months to 45 years) and the participant’s physiotherapists described their pain conditions as

resulting primarily from posture/tension/repeated strain (n=9), whiplash (n=7), degeneration

(n=5), trauma (n=2) and scoliosis (n=1). Participants were mildly to moderately disabled

(Neck Pain Disability Index score ± SD = 29% ± 13%). Participants were recruited through

local physiotherapy clinics and were reimbursed AU$20 for their participation. Participants

were excluded if they had pain-free neck rotation, were unable to tolerate repeated rotation to

the first onset of pain, had severely impaired vision, were under the age of 18 or if their

physiotherapist had identified significant neurological impairments such as sensory or motor

deficits and easily provoked, constant or progressive upper limb dysaesthesia. The protocol


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was approved by the Human Research Ethics Committee of the University of Suth Australia

(Protocol number: 31537).

Stimulus material and apparatus

A VR technique known as ‘re-directed walking’ modulates visual-proprioceptive

feedback by tracking real-world movement and then feeding this back into the virtual

environment in under- or over-stated form, creating the illusion of more or less movement

than is actually happening. Within certain limits, participants remain unaware of the

manipulation (Steinicke, Bruder, Jerald, Frenz, & Lappe, 2008). An Oculus Rift VR Head

Mounted Display (HMD) designed for immersive VR environments was used. The HMD

shown in Figure 1 displayed a virtual world and recorded head movement using internal

gyroscopes. Customised software was used to apply the selected rotation gains and map each

of six scenes to the virtual template. The six scenes included four outdoor scenes (a park, a

mountain, a countryside and church grounds) and two indoor scenes (a dining room and a

living room).


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Fig 1. Set-up of the VR experiment showing a supportive chair with trunk fixation,

headphones, head mounted display and the 360o (cylindrical) virtual template which

accommodated the six virtual scenes.

Experimental design

The study had a within-subject, randomised, double-blinded, repeated-measures

design. The range of neck rotation to the first onset of pain was quantified in three conditions

where virtual rotation was (a) 20% less than (rotation gain = 0.8), (b) equal to (rotation gain =

1) or (c) 20% greater than (rotation gain = 1.2) actual physical rotation. The order of the

three conditions was counterbalanced among participants, creating six possible orders. Four

participants were assigned to each of these counterbalancing orders according to a pre-

randomised order. Participants were blinded to the experimental manipulation and study

purpose, and the files relating to the three VR conditions were coded, thereby blinding the

experimenter to the order of conditions. The measurement of neck rotation was automated

and data were only extracted after all the data had been collected (A.I.).

Measurement

Axial neck rotation to the onset of pain was measured in degrees. Because

participants stopped at the first onset of pain in each trial, the range of motion to onset of pain

was defined as the peak rotation for each trial. This measure was extracted from each

automated trial output by a blinded assessor (A.I.).

Protocol

In order to prevent changes in postural alignment and to isolate neck movement,

subjects were seated in a supportive chair with the torso fixed in place by a seatbelt at the

level of the shoulders (see Figure 1). A laser pointer was fixed to the HMD and used to mark


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the starting position on the wall as a physical reference point for ‘zeroing’ of the gyroscopes

between measures and conditions. Participants wore white noise-emitting headphones to

counter any incidental noise, which might inform head orientation and disrupt the illusion.

For each of the three conditions, participants were asked to rotate slowly to the left,

stopping at the very first onset of pain, and then to return to the centre. Once the head had

returned to centre, the next trial was loaded and the task repeated to the right. Each condition

consisted of six left-rotation and six right-rotation measures. After each condition,

participants were asked to rate the average pain intensity experienced, for each rotation

direction to allow for subsequent assessment of any overall differences in pain intensity

between conditions. A 0-10 numerical rating scale (NRS) was used with anchors 0 = no pain

and 10 = the worst imaginable pain. To minimise the possibility that subjects would become

aware of the different rotation settings and thus directly compare them, each condition was

separated by a three-minute interval. In addition, six changing VR scenes acted as a decoy

from the actual study purpose and reduced the risk of participants’ anchoring their rotation to

a previous visual cue within a VR scene. In order to assess blinding, participants were asked

on completion of the experiment if they noticed anything different between the three

conditions.

Manipulation check 1: Setting boundaries for altered visual-proprioceptive feedback

VR operates by tracking real-world changes in orientation and applying this to the

virtual world being experienced via the HMD. The ‘rotation gain’ (the factor by which real

rotation is translated to virtual rotation) can be manipulated such that virtual and physical

rotation differ. In order to blind participants to this manipulation, the upper and lower limits

of the rotation gain were based on the results of a pilot study. During this pilot study, an

independent cohort of nine healthy participants (7 males; Mage= 32 years, SDage= 12) were


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presented with a range of rotation gain settings and asked to rotate their heads. They were to

indicate when a difference between real and virtual rotation occurred by judging the observed

rotation as slower than, equal to, or faster than their true physical rotation. We aimed to

determine the rotation gain at which participants were more likely to judge the virtual and

real rotation to be equal than they were to judge them to be different. As shown in Figure 2,

the rotation gains that corresponded to these points were 0.72 and 1.18. As a result, our

experimental gain settings were chosen to fall between 0.8 and 1.2, and additional controls

were implemented to ensure that participants in the main study remained blinded.

Fig 2. The percentage of rotation trials rated as slow, equal or fast for each rotation gain

setting. * indicates the range of rotation gain settings where virtual and real-world movement

speeds were perceived as being equal more often than faster or slower.

Manipulation check 2: Reliability and validity of measurement

The reliability of the gyroscopic measurement of rotation was tested by attaching the

HMD to a mechanical (goniometric) arm and testing its ability to repeatedly and accurately

0

10

20

30

40

50

60

70

80

0.6 0.7 0.8 0.9 1.0 1.1 1.2 1.3

Slow

Equal

Fast

Rotation gain

% o

f ro

tati

on

s ra

ted

slo

w,

eq

ua

l a

nd

fa

st

*


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measure three set angles (20o, 40o, and 60o). Initial observation of repeated measures

revealed that while the measurement was highly precise over a small number of trials, it

gradually drifted with more trials. Therefore, a protocol was developed which required the

virtual compass to be ‘zeroed’ every 5 trials. To further prevent accumulation of error, the

programme was refreshed between conditions. This protocol was found to have a correlation

with actual rotation of r = .994, and a high degree of precision for repeated measures at

20o(M = 19.8o, SD = 0.8o), 40o (M = 39.6o, SD = 0.3o) and 60o (M = 59.1o, SD = 2.5o).

Data extraction and statistical analysis overview

In order to test the main hypothesis that visual information that overstates or

understates true rotation can affect movement-evoked pain, we compared the range of motion

to first onset of pain between the three conditions, using repeated-measures ANOVA with

Bonferroni-corrected pairwise comparisons. In order to account for between-subject

differences in range of motion, data for each participant were transformed to ‘a proportion of

the average range of motion demonstrated in the neutral condition’. Alpha was set at p <

0.05 and the effect sizes partial eta squared (��) and Cohen’s d were interpreted with respect

to Cohen’s guidelines (0.01 = small, 0.059 = medium and 0.138 = large; and 0.2 = small, 0.5

= medium, 0.8 = large respectively) (Cohen, 1988). As a manipulation check, each

participant’s average movement-evoked pain for each condition was normalised to a

proportion of their average across conditions. Normalised pain ratings were then compared

between conditions using repeated-measures ANOVA.


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Results

Primary outcome: Range of motion to pain onset

The repeated-measures ANOVA revealed a large overall effect of visual-

proprioceptive feedback (Condition) on pain-free range, F(2, 135) = 18.35, p < .001, �� =

0.214. All pairwise comparisons were significant (p < .014). When vision understated true

rotation, there was a medium effect toward increased range of motion to the first onset of

pain, p = .014, d = 0.65; and when vision overstated true rotation, there was a large effect,

this time, toward decreased range of motion to the first onset of pain, p = .005, d = 0.83. That

is, the visual feedback was able to delay the onset of pain by 6% (CI 2-11%) or advance it by

7% (CI 4-11%), showing an overall manipulation of 13%.

Feedback suggests

less movement

Feedback matches

movement

Feedback suggests

more movement

Me

an

ra

ng

e o

f m

oti

on

to

pa

in o

nse

t

(95

% C

I)

0.90

0.95

1.00

1.05

1.10


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Fig. 4. Mean (circle) and 95% confidence interval (error bars) for the range of motion to

first onset of pain presented as a proportion of the mean range of rotation for the neutral

condition.

Pain intensity across conditions

The repeated-measures ANOVA did not reveal any difference in pain intensity

between conditions (p = 0.6). That is, any difference in rotation could not be explained by

participants’ actually moving beyond or stopping short of their pain threshold, which

strengthens our confidence in the main finding. In fact, inspection of Figure 3 hints at more

pain in the condition where visual feedback suggested more movement, further reinforcing

the finding that the visual suggestion of more movement increases sensitivity.

Fig. 3. Mean (circles) and 95% confidence interval (error bars) for the normalised pain

ratings reported for neck rotation in each condition.

Feedback suggests

less movement

Feedback matches

movement

Feedback suggests

more movement

Av

era

ge

pa

in r

ati

ng

(95

% C

I)

0.950

0.975

1.000

1.025

1.050


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Discussion

We examined how altering visual-proprioceptive feedback during neck rotation affects the

range of motion to the onset of pain (the movement-evoked pain threshold) in longstanding

neck pain sufferers. Using the ‘information-based’ view of pain, we hypothesised that pain

would occur at a lesser degree of head rotation when visual-proprioceptive information

overstated true rotation, and at a greater degree when visual-proprioceptive information

understated true rotation. The hypothesis was clearly supported – visual feedback that

overstated neck rotation resulted in pain onset occurring at a lesser degree of movement

(reduced pain threshold), whereas visual feedback that understated neck rotation resulted in

pain onset occurring at a greater degree of movement (increased pain threshold). The finding

that visual-proprioceptive cues may contribute to a pain-evoking sensory suite is particularly

relevant because chronic pain is most commonly provoked by particular movements and

body positions.

Our results appear consistent with the view of pain as the perceptual result of the

brain’s inference that body tissue is in danger (Merksey & Bogduk, 1994; Moseley, 2003;

Price, 1999; Arntz & Claassens, 2004) and corroborate related evidence of the relationship

between experienced pain intensity and cues that imply threat to tissue (Arntz & Claassens,

2004; Atlas & Wagner 2012; Moseley & Arntz, 2007; Wiech et al., 2010). For example, a

noxious cold stimulus evokes more pain if it is accompanied by a red light than if it is

accompanied by a blue one (Moseley & Arntz, 2007); a noxious laser stimulus evokes more

pain, and different cortical activation, if it is delivered to an area of skin thought by the

participant to be ‘thinner than normal’ than if it is delivered to skin thought to be normal

(Wiech et al., 2010). Such examples offer compelling evidence that pain can be modulated if

there is credible evidence of tissue danger, even if that evidence is not from the nociceptive


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domain. The current results offer a new direction however, because they show a shift in pain

threshold, rather than an upregulation of pain. This is important because most examples of

amplification of pain can be explained by enhanced senstivity within the nociceptive system

– most notably termed ‘central sensitisation’. We contend that our results, of a reduced pain

threshold to movement, are very unlikely due to central sensitisation because that would be

more likely to manifest in the opposite result – greater pain increase in response to greater

magnitude of movement. We contend that the most obvious explanation for the current

results is associative learning. That is, neck rotation involves a suite of motor, visual and

proprioceptive processes that, for the person with neck pain, becomes associated with

nociceptive input, such that the non-nociceptive aspects of the sensorial suite are sufficient to

trigger pain with or without the nociceptive component.

That the effect clearly relies on visual input triggering some sort of ‘threat threshold’,

does not exclude the possibility that non-cortical mechanisms are involved. Most obvious

here is the descending modulatory system, whereby primarily brainstem nuclei exert both

inhibitory and facilitatory influences over dorsal horn neurones (see Woolf & Slater, 2006 for

review). According to modern models of pain, however, the evaluative processes that

subserve descending modulation are grounded in those that subserve the production of pain

itself. That is, pain can be considered to reflect the perceived need to protect body tissue;

descending modulation can be considered a ‘correction’ of spinal nociceptor activity (i.e. the

‘danger message’) so as to bring it into line with the brain’s evaluation of true danger (see

Moseley, 2007; Butler, 2013; Fields, 2006). This understanding is analogous to that applied

to motor control, whereby motor commands are corrected according to somatosensory and

visual feedback (Sperry, 1950; Von Holst, 1950). Those models are also relevant here

because it is also possible that the bogus visual feedback modulates proprioceptive sensitivity

(Gandevia, Refshauge & Collins, 2002), which in turn may modulate nociceptive input.


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Notably, the pain advancing effect of overstating rotation was greater than the pain

delaying effect of understating rotation, indicating that visual feedback had a greater ability to

advance than delay pain. This finding fits with the greater potential cost of a perceptual error

that delays the onset of pain, which is consistent with inferential perceptual models (i.e.

Bayesian) that include a cost function (Feldman, 2013; Tabor, Catley, Gandevia, Thacker, &

Moseley, 2013).

Although the current work was experimental in nature, it raises intriguing potential

clinical implications. First, our results clearly suggest a rethink of how we interpret simple

clinical tests such as movement-evoked pain. Such tests are widely held to reflect sensitivity

of tissues and nociceptive pathways – repeatable and stable movement-evoked pain

thresholds are considered to be consistent with a primary nociceptive driver of pain – the

presence of tissue pathology (Jones & Rivett, 2004). However, our results suggest that this is

a naïve perspective. As such, it is not unreasonable to suggest that a VR set-up such as that

used here might play a role in the assessment of people in pain, to identify and quantify the

role of non-nociceptive somatosensory cues in pain and impairment. Second, if cues

signalling danger amplify or indeed trigger pain, then these cues present a novel target for

therapy. One way to extinguish the effect of such cues on pain might be to experientially

dissociate them from pain. For example, the re-directed walking techniques used in this

study can provide the illusory experience of large movements, but limit real-world movement

and pain. This idea might also be relevant to the use of visual illusory movements

administered by a mirror – common interventions for chronic limb pain conditions including

phantom limb pain and complex regional pain syndrome (Moseley, 2004; Moseley, 2006;

Ezendam, Bongers & Jannik, 2009; Bowering et al., 2012; Daly & Bialocerkowski, 2009) use

mirror-therapy, but the idea of distorting the feedback as a method of disentangling non-

nociceptive movement-related cues appears to have not been considered.


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The relationship observed here, between potentially threatening information and

movement-evoked pain, might also provide insight as to why cognitive and behavioural

interventions, such as education and exposure, which target perceived threat/pain-related fear,

also positively alter the relationship between movement and pain (Moseley, 2004; Vlaeyen,

de Jong, Geilen, Heuts, & van Breukelen, 2002). Whilst education, for example, may aim to

convince a patient that their pain is not a direct correlate of tissue stress, demonstrating this

with real-time evidence that their pain depends on visually encoded movement not actual

movement, may have therapeutic power.

Further research using the current framework might exploit more immersive and

multisensory VR, which may enable the delivery of more convincing and multimodal illusory

evidence of danger to the body. Further studies could also investigate how visual-

proprioceptive and other cues might acquire the ability to modulate/mediate pain (i.e. through

associative learning) as well as investigate why the effect might persist or over-generalise,

and how it might be extinguished. Disentangling pain from nociception is a challenge that

has been identified in experimental and cognitive psychology research (Moseley, 2012), but

the methodology used here lays a platform from which this challenge might be taken on.

Conclusion

In people with neck pain, when visual-proprioceptive feedback overstates true neck

rotation, neck pain occurs at a lesser degree of head rotation. When visual-proprioceptive

feedback understates true neck rotation, neck pain occurs later. We conclude, then, that

visual-proprioceptive information modulates pain threshold during head rotation in people

with neck pain. This has broad implications for our view of pain as an ‘information-evoked’

response and supports further investigation of non-nociceptive contributions to long-standing


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pain. Furthermore, the methodology outlined here presents a new method for theoretical and

experimental interrogation of pain, and raises the possibility of novel assessment and

therapeutic applications.

Author contributions

D.S.H and G.L.M. developed the study concept, contributed to design, data analysis,

interpretation and write-up. D.S.H. collected the data. V.J.M. contributed to study design and

write-up. M.B. and R.T.S contributed to study design and provided technical expertise for the

VR set-up. A.M. contributed to interpretation and write-up. All authors approved the final

version of the manuscript for submission.

References

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Arntz, A., & Claassens, L. (2004). The meaning of pain influences its experienced intensity. Pain,

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Bogus Visual Feedback Alters Onset of Movement-Evoked Pain in People With Neck Pain

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